Phylogenetic relationships of the New World titi monkeys (Callicebus): first appraisal of taxonomy based on molecular evidence

Abstract

BackgroundTiti monkeys, Callicebus, comprise the most species-rich primate genus—34 species are currently recognised, five of them described since 2005. The lack of molecular data for titi monkeys has meant that little is known of their phylogenetic relationships and divergence times. To clarify their evolutionary history, we assembled a large molecular dataset by sequencing 20 nuclear and two mitochondrial loci for 15 species, including representatives from all recognised species groups. Phylogenetic relationships were inferred using concatenated maximum likelihood and Bayesian analyses, allowing us to evaluate the current taxonomic hypothesis for the genus.ResultsOur results show four distinct Callicebus clades, for the most part concordant with the currently recognised morphological species-groups—the torquatus group, the personatus group, the donacophilus group, and the moloch group. The cupreus and moloch groups are not monophyletic, and all species of the formerly recognized cupreus group are reassigned to the moloch group. Two of the major divergence events are dated to the Miocene. The torquatus group, the oldest radiation, diverged c. 11 Ma; and the Atlantic forest personatus group split from the ancestor of all donacophilus and moloch species at 9–8 Ma. There is little molecular evidence for the separation of Callicebus caligatus and C. dubius, and we suggest that C. dubius should be considered a junior synonym of a polymorphic C. caligatus.ConclusionsConsidering molecular, morphological and biogeographic evidence, we propose a new genus level taxonomy for titi monkeys: Cheracebus n. gen. in the Orinoco, Negro and upper Amazon basins (torquatus group), Callicebus Thomas, 1903, in the Atlantic Forest (personatus group), and Plecturocebus n. gen. in the Amazon basin and Chaco region (donacophilus and moloch groups).Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0142-4) contains supplementary material, which is available to authorized users.

Ecological and Behavioural Factors Influencing Territorial Call Rates for the Bolivian Titi Monkeys, Plecturocebus modestus and Plecturocebus olallae

“…Nevertheless, if forest fragmentation occurs at high levels, the dramatic reduction of suitable habitat could result in the isolation of groups [Isabirye-Basuta and Lwanga, 2008], reducing their interactions, and also the rates of territorial calls. Robinson et al [1987] found that groups of titi monkeys (cited as Callicebus moloch , now considered Plecturocebus ornatus following Byrne et al [2016]) with small home ranges (HRs; ≤ 4 ha) tend to emit territorial calls from border areas of their territories, while conspecifics with larger HRs did that from central zones. Theoretically, smaller HRs lead to strong spatial competition, demanding intensive patrolling along territory boundaries where frequent group encounters promote high rates of territorial calls.…”

“…Nevertheless, this correction factor is often unknown, and some studies have deduced or extrapolated call rates from other species [Brockelman and Ali, 1987;Nijman and Menken, 2005;Höing et al, 2013]. For example, the territorial calls of the Beni titi monkey (Plecturocebus modestus) and Olalla brothers' titi monkey (P. olallae) , primates endemic to Bolivia (formerly: Callicebus modestus and C. olallae , respectively [Lönnberg, 1939;Hershkovitz, 1990;Felton et al, 2006;Martinez and Wallace, 2007, 2013Byrne et al, 2016]), both categorized as Endangered [Veiga et al, 2008a, b], were used to assess population density and size, but due to a lack of behavioural information the correction factor was estimated from short observations [López-Strauss, 2008;López-Strauss and Wallace, 2015].…”

An annotated checklist of the mammals of Paraguay

“…Plecturocebus pallescens Thomas 1907 X TXNM: as Callicebus donacophilus in Myers et al (2002), species clarification updated in Groves (2005), and family and generic clarification updated by Byrne et al (2016).…”

Pliocene Primates

“…Fossil and molecular evidence indicate that the three major clades of modern platyrrhines were established in the Miocene (Kay 2015), but as in other groups of primates, further divergence subsequently occurred. In titi monkeys, for example, the Pliocene saw the split between the donacophilus and moloch groups (Byrne et al 2016). The Pliocene also witnessed an important dispersal of monkeys northwards into Central America, made possible by the connection through the Isthmus of Panama between the continents of South and North America around 3.5 Ma (Kay 2015).…”